Kidney transplantation (KT) is the most obvious method of treating a patient with end-stage renal disease. In the early stages of KT, urine production is considered a marker of successful reperfusion of the kidney after anastomosis. However, there is no clear conclusion about the relationship between initial urine output after KT and 1-year renal function. Thus, we investigated the factors that affect 1-year kidney function after KT, including urine output.
Kim et al BMC Anesthesiology (2019) 19:231 https://doi.org/10.1186/s12871-019-0904-6 RESEARCH ARTICLE Open Access A retrospective study of the relationship between postoperative urine output and one year transplanted kidney function Joungmin Kim, Taehee Pyeon, Jeong Il Choi, Jeong Hyeon Kang, Seung Won Song, Hong-Beom Bae* Seongtae Jeong* and Abstract Background: Kidney transplantation (KT) is the most obvious method of treating a patient with end-stage renal disease In the early stages of KT, urine production is considered a marker of successful reperfusion of the kidney after anastomosis However, there is no clear conclusion about the relationship between initial urine output after KT and 1-year renal function Thus, we investigated the factors that affect 1-year kidney function after KT, including urine output Methods: This retrospective study investigated the relationship between urine output in the days after KT and transplanted kidney prognosis after 1-year In total, 291 patients (129 living-donor and 162 deceased-donor transplant recipients) were analyzed; 24-h urine volume per body weight (in kilograms) was measured for days postoperatively The estimated glomerular filtration rate (eGFR), determined by the Modification of Diet in Renal Disease algorithm, was used as an index of renal function Patients were grouped according to eGFR at 1-year after KT: a good residual function group, eGFR ≥60, and a poor residual function group, eGFR < 60 Result: Recipients’ factors affecting 1-year eGFR include height (P = 0.03), weight (P = 0.00), and body mass index (P = 0.00) Donor factors affecting 1-year eGFR include age (P = 0.00) and number of human leukocyte antigen (HLA) mismatches (P = 0.00) The urine output for days after KT (postoperative day 1; and 3) was associated with 1-year eGFR in deceased-donor (P = 0.00; P = 0.00 and P = 0.01) And, postoperative urine output was associated with the occurrence of delayed graft function (area under curve (AUC) = 0.913; AUC = 0.984 and AUC = 0.944) Conclusion: Although postoperative urine output alone is not enough to predict 1-year GFR, the incidence of delayed graft function can be predicted Also, the appropriate urine output after KT may differ depending on the type of the transplanted kidney Trial registration: Clinical Research Information Service of the Korea National Institute of Health in the Republic of Korea (KCT0003571) Keywords: Kidney transplantation, Urine output, Graft survival, Glomerular filtration rate * Correspondence: nextphil2@hanmail.net; anesjst@jnu.ac.kr Department of Anesthesiology and Pain Medicine, Chonnam National University Medical School; Chonnam National University Hospital, 42 Jebong-ro Dong-gu, Gwangju 61469, South Korea © The Author(s) 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated Kim et al BMC Anesthesiology (2019) 19:231 Background The incidence of end-stage renal disease (ESRD) is increasing with the prolonged life span and raised prevalence of chronic diseases, such as diabetes and hypertension [1] Kidney transplantation (KT) is a proven approach to improve quality of life and prolong life expectancy in patients with ESRD [2] Therefore, it has become important to maintain the function of the transplanted kidney due to the imbalance caused by limited supply and increasing demand During KT, recipients have been given mannitol [3], dopamine [4], furosemide [5], and fluid loading [6] to enhance transplanted-kidney function A few of these measures have increased the long-term survival rate of transplanted organs Early detection and prevention of renal functional decline are important for the maintenance of normal graft function Several tests, including urine-based measurements, can be used to evaluate the function of the kidneys Urine tests are suitable for clinical applications because the necessary samples are easy to obtain They involve the measurement of specific substances in the urine, such as kidney injury molecule-1 [7], or measurement of the urine volume In early stages of KT, urine production is considered to be a sign of successful reperfusion after anastomosis [8, 9] The use of perioperative diuretics to increase urine volume differs among centers with respect to type and dose [10, 11] Some reports have shown that long-term prognosis can be predicted by urine volume after KT [12, 13] However, excessive diuresis may occasionally result in a lack of circulating plasma volume or electrolyte imbalances [14] In general, it is known that the glomerular filtration rate (GFR) is an excellent indicator of overall kidney function [15] GFR measurements using exogenous markers such as inulin clearance are known to be the most accurate methods However, use of these markers is laborious and expensive, and thus is rare in clinical practice Conversely, although there is some inaccuracy, endogenous markers such as serum creatinine (Cr) or cystatin C are used to assess kidney function Limiting factors for using Cr as a marker of GFR include weight, age, sex and race The Modification of Diet in Renal Disease (MDRD) equation for GFR estimation was derived from 1628 patients with chronic kidney disease (mean GFR, 40 mL / / 1.73 m2) to overcome some limitations [16] Transplanted kidneys are known to produce large amounts of urine in the initial stage after transplantation [17] No criterion for the appropriate urine volume after KT has been established We aimed to compare urine volume in the days after surgery and the estimated glomerular filtration rate (eGFR) at year postoperatively in patients who received KT Page of 10 Methods Study design and ethical statement This single-center retrospective cohort study was conducted using the electronic medical records of Chonnam National University Hospital This registry retrospectively collects data regarding recipients’ characteristics and outcomes Adult patients (age ≥ 20 years) who underwent KT in our center during the 10-year period between January 2008 and 31 December 2017 were included The institutional review board of Chonnam National University Hospital approved the study protocol (CNUH-2019-018), and the study was registered with the Clinical Research Information Service of the Korea National Institute of Health in the Republic of Korea (KCT0003571), which belongs to the World Health Organization Registry Network Data collection In total, 303 kidney transplants, including re-transplantations, were performed during the study period Patients were excluded from the analysis if they lacked medical records for the first year after surgery, due to death or loss to follow-up; patients aged < 20 years were also excluded The preoperative information collected was age, sex, height, weight, body mass index (BMI), duration of dialysis, method of dialysis, eGFR, diabetes mellitus (DM) status, hypertension (HTN) status, hepatitis B virus status, hepatitis C virus status, and type of donated kidney eGFRs were estimated using the MDRD equation In addition, the characteristics of donated kidney such as age, Creatinine, DM, HTN, and human leukocyte antigen (HLA) mismatch, incidence of delayed graft function (DGF) were also investigated DGF was defined as hemodialysis performed within week after surgery Nephropathy was defined as primary kidney disorder, such as IgA nephropathy or autosomal polycystic kidney, but not secondary kidney disorder due to HTN or DM Our hospital usually measures the amount of urine for 24 h during the days after KT; those data were used in the present study The total volume (in milliliters) of urine collected over 24 h was divided by the body weight (in kilograms) of the patient Follow-up data (e.g., eGFR, graft rejection, and viral infection) were collected at year after KT Graft rejection episodes were defined as biopsy-proven rejection or clinically suspected acute rejection that was improved by empirical steroid pulse therapy Patients were considered to be positive for viral infection when cytomegalovirus (CMV), Epstein–Barr virus (EBV), or BK polyomavirus (BKV) was detected after KT Outcomes Chronic kidney disease (CKD) is defined as GFR < 60 mL/min/1.73 m2 for months or more [18] This criterion can be applied to KT patients [19] and, the degree of GFR impairment at year post-KT has prognostic value and is associated with lower GFR at years, higher risk Kim et al BMC Anesthesiology (2019) 19:231 of eventual graft failure, and cardiovascular death [20] The patients were grouped according to eGFR at year after KT: a good residual function group, eGFR ≥60, and a poor residual function group, eGFR < 60 The primary goal was to assess the relationship between the eGFR at year postoperatively and urine output during the days after KT The secondary goal was to assess the association of eGFR at year after KT with other patient data, such as donated kidney’s demographics, fluid and diuretic dose, rejection and infection Statistical analysis For demographic data, the independent two sample ttest for normal continuous data or the Wilcoxon ranksum test for non-normal continuous data were used as appropriate The normality was verified by Shapiro-Wilk test The categorical data was analyzed by the Chisquared test or Fisher’s Exact test A subgroup analysis according to the type of transplanted kidney was performed A bonferroni correction was used to adjust type I error for multiple comparisons in subgroup analysis and P values 90%, and this rate is gradually improving for deceaseddonor KT [29] However, the 20-year transplanted kidney survival rate is 21% [30] The method of raising the long-term survival rate of transplanted kidney is avoidance of known risk factors Donor risk factors associated with graft failure are age > 60 years, history of HTN, cerebrovascular cause of death, and pre-harvest serum Cr > 150 mol/L [31] Risk factors measured in this study were age, hypertension and HLA mismatch Recipient risk factors associated with graft failure include age, Table Relationship of residual kidney function and postoperative furosemide dosage (mg) of 1st, 2nd, and 3rd day P value Good residual function group Poor residual function group (n = 179) (n = 112) POD1 40 [20; 80] 40 [20; 80] 61 POD2 40 [20; 80] 40 [20; 60] 31 POD3 20 [20; 40] 20 [20; 40] 08 All Living donor kidney (n = 84) (n = 45) POD1 40 [20; 80] 40 [20; 80] 69 POD2 60 [40; 100] 60 [40; 80] 56 POD3 20 [20; 40] 20 [20; 40] 21 (n = 95) (n = 67) POD1 60 [20; 80] 40 [20; 60] 17 POD2 20 [20; 60] 20 [20; 60] 68 POD3 20 [20; 40] 20 [20; 40] 20 Deceased donor kidney Data are present as median [95% confidence interval] Good residual function group: year eGFR ≥60, Poor residual function group: year eGFR < 60 POD Postoperative day Kim et al BMC Anesthesiology (2019) 19:231 Page of 10 Table Relationship of residual kidney function and postoperative mannitol dosage (g) of 1st, 2nd, and 3rd day P value Good residual function group Poor residual function group (n = 179) (n = 112) POD1 30 [30; 30] 30 [30; 30] 51 POD2 30 [30; 30] 30 [30; 30] 39 POD3 [0; 30] 30 [0; 30] 28 All Living donor kidney (n = 84) (n = 45) POD1 30 [30; 30] 30 [0; 30] POD2 30 [30; 30] 30 [30; 30] 35 POD3 [0; 30] [0; 30] 85 (n = 95) (n = 67) POD1 30 [30; 30] 30 [30; 30] 49 POD2 30 [30; 30] 30 [30; 30] 83 POD3 30 [0; 30] 30 [0; 30] 44 65 Deceased donor kidney Data are present as median [95% confidence interval] Good residual function group: year eGFR ≥60, Poor residual function group: year eGFR < 60 POD Postoperative day increasing plasma renin activity, BMI, prior transplant, dialysis at the time of KT, and hepatitis C virus infection [32] Our study also showed that recipient height, weight and BMI affect graft function Navis et al [33] reported that increased BMI was associated with increased glomerular filtration pressure, which adversely affected longterm graft survival In this study, postoperative viral infection was associated with the 1-year eGFR There may be several types of viral infections after KT, but CMV and BKV are common Viral infections may affect acute or chronic rejection episodes Reportedly, 72% of CMV-positive recipients developed rejection, whereas CMV-negative recipients had only a 17% rejection rate [34] The mechanism of CMV-induced allograft rejection is as follows First, activation of HLA class I antigen-specific T cells due to cross-reactivity with CMV antigens Second, release of inflammatory cytokines [eg, IL (interleukin) -1, IL-6, IL-8, and tumor necrosis factor-α] and direct damage of endothelial cells Third, these complex interactions not only increase the expression of HLA class II molecules in allogeneic grafts, but also produce adhesion molecules of white blood cells and endothelial cells [35] Finally, the results of this study show a correlation between the occurrence of rejection episodes and the 1year eGFR Esteve et al [36] reported that patients with rejection episodes were at increased risk of late graft failure In addition, acute rejection episodes affected graft survival, regardless of the time of onset [37] Immunosuppressant use is inevitable in KT patients to achieve control of rejection, but it renders the recipient susceptible to viral infection and reactivation [38] Table Predicting DGF incidence with postoperative urine output using ROC curve AUC POD1UO 0.913 POD2UO 0.984 POD3UO 0.944 POD1UO + + 0.969 AUC Area under curve, PODUO Post-operative day urine output Fig ROC curve of urine output POD1–3 for year eGFR (POD = postoperative day) Kim et al BMC Anesthesiology (2019) 19:231 Page of 10 Table Rejection episode Good residual function group Poor residual function group (n = 179) (n = 112) (5%) 33 (29%) 170 (95%) 79 (71%) P value All Positive 00 Negative Living donor kidney Positive (n = 84) (n = 45) (7%) 16 (36%) 78 (93%) 29 (64%) 00 Negative Deceased donor kidney (n = 95) Positive (n = 67) (3%) 17 (25%) 92 (97%) 50 (75%) 00 data are different between the groups (for example BMI), so we tried to compensate for this difference by using urine volume per weight rather than postoperative urine output itself Third, The incidence of DGF in this study was lower than in other studies [39] This may reveal that postoperative urine output is a risk factor for the development of DGF, but is insufficient to explain the outcome of year eGFR Fourth, we used eGFR with MDRD to assess kidney function This formula tends to be somewhat higher than the actual glomerular filtration rate in Asians, including Japan, and suffers from a slight drop in accuracy when glomerular filtration rate is normal or slightly decreased [40] But, the MDRD equation was the most accurate of the creatinine-based equations [41] Fifth, we did not analyze post-transplantation blood pressure control statuses of the recipients or the types of immunosuppressive drug used after KT Negative Data are present as number (%) Good residual function group: year eGFR ≥60, Poor residual function group: year eGFR < 60 In the present study, most KT were carried out by one surgeon and there were few variables due to surgery However, this study has the following limitations First, this study was retrospectively conducted in a single institution Therefore, the sample size was small and there was no direct measurement of renin and aldosteron However, it is known that renin and aldosterone levels are raised in deceased donor KT Second, demographic Conclusions Sufficient urine output after immediate KT reflects proper blood supply to the transplanted kidney and the absence of stenosis or leakage at the anastomosis site Early postoperative urine output was associated with 1year postoperative graft function in deceased-donor kidney recipients, but not in living-donor kidney recipients This difference may be caused by activation of the RAAS due to prolonged cold ischemic time during the preparation of deceased-donor kidneys Therefore, we recommend that the approach to achieving proper urine volume after KT be adjusted depending on the type of transplanted kidney Table Viral infection Good residual function group Poor residual function group (n = 179) (n = 112) P value All Positive 19 (11%) 35 (31%) 160 (89%) 77 (69%) 00 Abbreviations BKV: BK poliomavirus; BMI: Body mass index; CMV: Cytomegalovirus; Cr: Creatinine; DGF: Delayed graft function; DM: Diabetes mellitus; EBV: Epstein-Barr virus; eGFR: Estimated glomerular filtration rate; ESRD: Endstage renal disease; HLA: Human leukocyte antigen; HTN: Hypertension; IL: Interleukin; KT: Kidney transplantation; MDRD: Modification of Diet in Renal Disease; POD: Postoperative day; RAAS: Renin-angiotensionaldosterone system; ROC: Receiver-operating-characteristic Negative 00 Acknowledgments The English in this document has been checked by at least two professional editors, both native speakers of English For a certificate, please see: http://www.textcheck.com/certificate/eZ5njx 01 Authors’ contributions HBB and SJ participated in study conception and supervision of the research group Manuscript editing JK was involved with manuscript drafting and interpretation JHK was involved with data analysis SWS was involved with statistical analysis and manuscript drafting TP was involved with manuscript editing JIC was involved with data interpretation All authors have read and approved the final manuscript Living donor kidney (n = 84) Positive (n = 45) (5%) 13 (29%) 80 (95%) 32 (71%) Negative Deceased donor kidney Positive (n = 95) (n = 67) 15 (16%) 22 (33%) 80 (84%) 45 (67%) Negative Data are present as number (%) Good residual function group: year eGFR ≥60, Poor residual function group: year eGFR < 60 Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sector Kim et al BMC Anesthesiology (2019) 19:231 Availability of data and materials The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request Ethics approval and consent to participate This single-center retrospective cohort study was approved by the institutional review board (IRB) of Chonnam National Universitiy Hospital (IRB approval number: CNUH-2019-018) The informed consent was waived because of the retrospective nature of this study Consent for publication Not applicable Competing interests The authors declare that they have no competing interest Received: 15 September 2019 Accepted: December 2019 References Hill NR, Fatoba ST, Oke JL, Hirst JA, O'Callaghan CA, Lasserson DS, et al Global prevalence of chronic kidney disease - a systematic review and meta-analysis PLoS One 2016;11(7):e0158765 Wolfe RA, Ashby VB, Milford EL, Ojo AO, Ettenger RE, Agodoa LY, et al Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant N Engl J Med 1999;341(23):1725–30 van Valenberg PL, Hoitsma AJ, Tiggeler RG, Berden JH, van Lier HJ, Koene RA Mannitol as an indispensable constituent of an intraoperative hydration protocol for the prevention of acute renal failure after renal cadaveric transplantation Transplantation 1987;44(6):784–8 Ciapetti M, di Valvasone S, di Filippo A, Cecchi A, Bonizzoli M, Peris A Lowdose dopamine in kidney transplantation Transplant Proc 2009;41(10): 4165–8 Lachance SL, Barry JM Effect of furosemide on dialysis requirement following cadaveric kidney transplantation J Urol 1985;133(6):950–1 Othman MM, Ismael AZ, Hammouda GE The impact of timing of maximal crystalloid hydration on early graft function during kidney transplantation Anesth Analg 2010;110(5):1440–6 Bonventre JV Kidney injury molecule-1 (KIM-1): a urinary biomarker and much more Nephrol Dial Transplant 2009;24(11):3265–8 Matteucci E, Carmellini M, Bertoni C, Boldrini E, Mosca F, Giampietro O Urinary excretion rates of multiple renal indicators after kidney transplantation: clinical significance for early graft outcome Ren Fail 1998; 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Prediction of DGF and year residual graft function through postoperative urine output Postoperative day urine output was the highest in the correlation between days postoperative urine output and DGF